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Delaying reproduction: the "disposable germline" hypothesis

This week's paper sheds new light on trade-offs between longevity and reproduction in Caenorhabditis elegans. This nematode worm is popular with medical researchers because it has a simple nervous system, insulin-like hormones, etc., yet it can be grown in Petri dishes, where it can mature and start reproducing two days after hatching from a tiny egg.

At various stages during this maturation process, C. elegans can essentially put life on hold. Environmental cues, particularly food shortage, switch them off their normal developmental pathway onto a side-track, where they can survive for months without food, but without maturing. Once food returns, they resume development.

This week's paper reports a new kind of developmental delay in individuals on the verge of reproductive maturity. "Starvation Protects Germline Stem Cells and Extends Reproductive Longevity in C. elegans" was published in Science, by Giana Angelo and Marc R. van Glist, working at the Fred Hutchison Cancer Resarch Center, in Seattle.

When worms with developing eggs are starved just before reproducing, some of them "die in childbirth", as the eggs hatch inside their bodies and emerge. Others, however, delay reproduction. Most of the developing germ cells apparently end up getting digested "for fuel", rather than becoming eggs. The adults can then survive for a month or more. Once fed, they resume reproduction, although they then lay fewer eggs than if they hadn't been starved. So an individual who would have started to lay eggs on day 2 can start on day 30 instead, a 15-fold delay in reproductive maturity.

Why do they do this? The authors have identified some genes that help control this process. But evolutionary biologists ask a different kind of "why" question: why have genes for delaying reproduction under starvation displaced genes for reproducing at the usual age?

A common answer is that they are waiting for "better conditions." But better how? Maybe they can produce more eggs if they wait until there's more food. But the relative success of different genes depends on the timing of reproduction, not just the number of offspring. An individual that produces a few eggs early might have lots of great-grandchildren by the time an individual who delayed reproduction started to lay eggs. A key point is that evolutionary changes in the genetic composition of populations depend on the relative performance of individuals with different genes. Maybe there will be more food later, but there will be more food later for everyone: for individuals who delayed reproduction and for the descendants of those who didn't.

It turns out that the one "better condition" that really makes it worthwhile to delay reproduction is a decrease in overall population size. -- not the increased resources per individual that you might get with lower population, but lower population itself. This is because each offspring added to a smaller gene pool will have a disproportionately large effect on the composition of future generations. As we put it in a recent paper, "When Stress Predicts a Shrinking Gene Pool, Trading Early Reproduction for Longevity Can Increase Fitness, Even with Lower Fecundity."

Under our "smaller pond" hypothesis, starvation provides worms with information, specifically, information predicting a decreasing population. That makes delaying reproduction a promising strategy. Even if the worm ends up laying fewer eggs (which isn't necessarily the case, depending on the direct effects of food supply on egg production), they will join a smaller gene pool. Individuals delaying reproduction will therefore be over-represented in future generations.

Food supply isn't the only factor predicting whether population will increase or decrease. If it's crowded, even a large food supply may not last long. Nematodes have previously been shown to detect the degree of crowding, essentially by smelling each other. Crowding can contribute to delays in maturation earlier in life. This week's paper shows that this is also true for adults that delay reproduction. If starved individuals are removed from the crowd, they resume reproduction, even without food. If there are few other worms around -- they probably can't tell the difference between "few" and "none" -- this is their big chance to found a dynasty.

The authors propose a "disposable germline" hypothesis. This is an allusion to Kirkwood's discredited "disposable soma" hypothesis, which attempted to explain trade-offs between reproduction and longevity as the result of limited resources: not enough calories to reproduce and also maintain healthy bodies. Although the "disposable soma" hypothesis has been cited hundreds of times, it hasn't been quite the same since people discovered that starvation increases longevity. To explain this result under the "disposable soma" hypothesis, you would have to assume that starving individuals save so many calories by not reproducing that they actually have more calories available for maintenance than if they had all the food they could eat.

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